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      Neural Variability and Sampling-Based Probabilistic Representations in the Visual Cortex

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          Summary

          Neural responses in the visual cortex are variable, and there is now an abundance of data characterizing how the magnitude and structure of this variability depends on the stimulus. Current theories of cortical computation fail to account for these data; they either ignore variability altogether or only model its unstructured Poisson-like aspects. We develop a theory in which the cortex performs probabilistic inference such that population activity patterns represent statistical samples from the inferred probability distribution. Our main prediction is that perceptual uncertainty is directly encoded by the variability, rather than the average, of cortical responses. Through direct comparisons to previously published data as well as original data analyses, we show that a sampling-based probabilistic representation accounts for the structure of noise, signal, and spontaneous response variability and correlations in the primary visual cortex. These results suggest a novel role for neural variability in cortical dynamics and computations.

          Highlights

          • Stochastic sampling links perceptual uncertainty to neural response variability

          • Model accounts for independent changes in strength and variability of responses

          • Model predicts relationship between noise, signal, and spontaneous correlations

          • Stimulus statistics dependence of response statistics is explained

          Abstract

          Orbán et al. show that linking perceptual uncertainty to neuronal variability accounts for systematic changes in variability and covariability in simple cells of the primary visual cortex. The theory also establishes a formal relationship between signal, noise, and spontaneous correlations.

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          Most cited references46

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          The importance of mixed selectivity in complex cognitive tasks.

          Single-neuron activity in the prefrontal cortex (PFC) is tuned to mixtures of multiple task-related aspects. Such mixed selectivity is highly heterogeneous, seemingly disordered and therefore difficult to interpret. We analysed the neural activity recorded in monkeys during an object sequence memory task to identify a role of mixed selectivity in subserving the cognitive functions ascribed to the PFC. We show that mixed selectivity neurons encode distributed information about all task-relevant aspects. Each aspect can be decoded from the population of neurons even when single-cell selectivity to that aspect is eliminated. Moreover, mixed selectivity offers a significant computational advantage over specialized responses in terms of the repertoire of input-output functions implementable by readout neurons. This advantage originates from the highly diverse nonlinear selectivity to mixtures of task-relevant variables, a signature of high-dimensional neural representations. Crucially, this dimensionality is predictive of animal behaviour as it collapses in error trials. Our findings recommend a shift of focus for future studies from neurons that have easily interpretable response tuning to the widely observed, but rarely analysed, mixed selectivity neurons.
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            Neural population dynamics during reaching

            Most theories of motor cortex have assumed that neural activity represents movement parameters. This view derives from an analogous approach to primary visual cortex, where neural activity represents patterns of light. Yet it is unclear how well that analogy holds. Single-neuron responses in motor cortex appear strikingly complex, and there is marked disagreement regarding which movement parameters are represented. A better analogy might be with other motor systems, where a common principle is rhythmic neural activity. We found that motor cortex responses during reaching contain a brief but strong oscillatory component, something quite unexpected for a non-periodic behavior. Oscillation amplitude and phase followed naturally from the preparatory state, suggesting a mechanistic role for preparatory neural activity. These results demonstrate unexpected yet surprisingly simple structure in the population response. That underlying structure explains many of the confusing features of individual-neuron responses.
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              The variable discharge of cortical neurons: implications for connectivity, computation, and information coding.

              Cortical neurons exhibit tremendous variability in the number and temporal distribution of spikes in their discharge patterns. Furthermore, this variability appears to be conserved over large regions of the cerebral cortex, suggesting that it is neither reduced nor expanded from stage to stage within a processing pathway. To investigate the principles underlying such statistical homogeneity, we have analyzed a model of synaptic integration incorporating a highly simplified integrate and fire mechanism with decay. We analyzed a "high-input regime" in which neurons receive hundreds of excitatory synaptic inputs during each interspike interval. To produce a graded response in this regime, the neuron must balance excitation with inhibition. We find that a simple integrate and fire mechanism with balanced excitation and inhibition produces a highly variable interspike interval, consistent with experimental data. Detailed information about the temporal pattern of synaptic inputs cannot be recovered from the pattern of output spikes, and we infer that cortical neurons are unlikely to transmit information in the temporal pattern of spike discharge. Rather, we suggest that quantities are represented as rate codes in ensembles of 50-100 neurons. These column-like ensembles tolerate large fractions of common synaptic input and yet covary only weakly in their spike discharge. We find that an ensemble of 100 neurons provides a reliable estimate of rate in just one interspike interval (10-50 msec). Finally, we derived an expression for the variance of the neural spike count that leads to a stable propagation of signal and noise in networks of neurons-that is, conditions that do not impose an accumulation or diminution of noise. The solution implies that single neurons perform simple algebra resembling averaging, and that more sophisticated computations arise by virtue of the anatomical convergence of novel combinations of inputs to the cortical column from external sources.
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                Author and article information

                Contributors
                Journal
                Neuron
                Neuron
                Neuron
                Cell Press
                0896-6273
                1097-4199
                19 October 2016
                19 October 2016
                : 92
                : 2
                : 530-543
                Affiliations
                [1 ]Computational and Biological Learning Lab, Department of Engineering, University of Cambridge, Cambridge CB2 1PZ, UK
                [2 ]MTA Wigner Research Center for Physics, Budapest 1121, Hungary
                [3 ]Volen National Center for Complex Systems, Brandeis University, Waltham, MA 02454, USA
                [4 ]Department of Cognitive Science, Central European University, Budapest 1051, Hungary
                [5 ]Brain & Cognitive Sciences, University of Rochester, Rochester, NY 14627, USA
                Author notes
                []Corresponding author orban.gergo@ 123456wigner.mta.hu
                [6]

                Lead Contact

                Article
                S0896-6273(16)30639-0
                10.1016/j.neuron.2016.09.038
                5077700
                27764674
                e6f57618-878d-44af-bb97-3c9e917ca4d0
                © 2016 The Author(s)

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 22 March 2016
                : 27 July 2016
                : 6 September 2016
                Categories
                Article

                Neurosciences
                vision,v1,variability,noise correlations,natural images,spontaneous activity,normative model,theory,stochastic sampling,bayesian computations

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